Dynamics of Bacterial Hand Contamination During Routine Neonatal Care

INFECTION C O N T R O L AND HOSPITAL EPIDEMIOLOGY March 2 0 0 4

DYNAMICS OF BACTERIAL H A N D CONTAMINATION

DURING ROUTINE NEONATAL CARE

Carmem Lucia Pessoa-Silva, MD; Sasi Dharan, MT; Stephane Hugonnet, MD, MSc; Sylvie Touveneau, RN; Klara Posfay-Barbe, MD; Riccardo Pfister, MD; Didier Pittet, MD, MS

A B S T R A C T

OBJECTIVE: To evaluate the dynamics of bacterial cont-amination of healthcare workers' (HCWs) hands during neonatal care.

SETTING: The 20-bed neonatal unit of a large acute care teaching hospital in Geneva, Switzerland.

METHODS: Structured observation sessions were con-ducted. A sequence of care began when the HCW performed hand hygiene and ended when the activity changed or hand hygiene was performed again. Alcohol-based handrub was the standard procedure for hand hygiene. An imprint of the five fin-gertips of the dominant hand was obtained before and after hand hygiene and at the end of a sequence of care. Regression meth-ods were used to model the final bacterial count according to the type and duration of care and the use of gloves.

RESULTS: One hundred forty-nine sequences of care

were observed. Commensal skin flora comprised 72.4% of all cul-ture-positive specimens (n = 360). Other microorganisms identi-fied were Enterobacteriaceae (n = 55, 13.8%); Staphylococcus aureus (n = 10, 2.5%); and fungi (n = 7, 1.8%). Skin contact, respi-ratory care, and diaper change were independently associated with an increased bacterial count; the use of gloves did not fully protect HCWs' hands from bacterial contamination.

CONCLUSIONS: These data confirm that hands become progressively contaminated with commensal flora and potential pathogens during neonatal care, and identify activities at higher risk for hand contamination. They also reinforce the need for hand hygiene after a sequence of care, before starting a different task, and after glove removal {Infect Control Hosp Epidemiol 2004;25:192-197).

Hand hygiene remains the single most important measure to prevent cross-transmission of microorganisms1 and reduces patient morbidity and mortality from nosocomi-al infections,23 a major complication of hospital care in the pediatric population.4"9 Nosocomial infections affect up to 30% of neonates,510"13 and rates can be more than five times higher in this population compared with older children.1011 Of major concern is the high proportion (approximately 40%) of bloodstream infections,14 which are associated with increased mortality, prolonged hospital stay, and slower growth among infants with very low birth weights.15"17

Compliance with hand hygiene recommenda-tions118 may be difficult to achieve when caring for neonates, particularly those who are hospitalized in intensive care units.19 Similar to other settings, observed compliance with hand hygiene has been reported as no better than 40%. Few studies, however, support current guidelines on indications for hand hygiene.20 Earlier guidelines present vague recommendations on indica-tions for hand hygiene and put the responsibility on the healthcare worker (HCW) to assess the risk of potential hand contamination and decide for or against hand

hygiene.20 Some studies suggest a ranking of patient care activities2122 that are likely to cause hand contamination as a tool to define hand hygiene indications, although such systems lack scientific validation.18 In particular, opportunities for adequate hand hygiene in the neonatal setting have not yet been defined.

We studied the dynamics of bacterial contamination of HCWs' hands during routine neonatal care to help iden-tify high-risk opportunities for hand contamination.

M E T H O D S Setting

The study was conducted from March 26 to April 9, 2001, in the neonatal unit of the University of Geneva Hospitals, a large referral institution providing primary and tertiary medical care for residents of Geneva, Switzerland, and the surrounding area (population of approximately 800,000).

The neonatal unit is divided into two sections located in separate areas: intermediate care consists of 3 patient care pods (12 beds) and intensive care consists of 2 pods (8 beds). Approximately 700 neonates (5,200 patient-days) are

Dr. Pessoa-Silva, Mr. Dharan, Dr. Hugonnet, Ms. Touveneau, and Dr. Pittet are from the Infection Control Program, Department of Internal Medicine and Drs. Posfay-Barbe and Pfister are from the Department of Pediatrics, University of Geneva Hospitals, Geneva, Switzerland.

Address reprint requests to Professor Didier Pittet, MD, MS, Director, Infection Control Program, Department of Internal Medicine, University of Geneva Hospitals, 24 Rue Micheli-du-Crest, 1211 Geneva 14, Switzerland.

Supported by a grant from the Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq), Nr 200694/99-5.

admitted annually to the unit. Handwashing facilities are conveniently located throughout, with one manual sink, medicated soap (chlorhexidine gluconate 4%), and paper towels inside every pod, and alcohol-based handrub solu-tion is widely available.23 The average patient-to-nurse ratio is 3:2 and 1:1 in the intermediate and intensive care sec-tions, respectively. Clinical staff includes 17 physicians and 84 registered nurses.

Definitions

Rubbing hands with an alcohol-based (75% vol/vol, isopropanol) preparation of chlorhexidine gluconate (0.5%) (Hopirub, B. Braun Medical AG, Sempach, Switzerland) was defined as the standard procedure for hand hygiene before and after patient care activities, unless hands were visibly soiled.18 In this case, HCWs performed handwash-ing with medicated soap (4% chlorhexidine gluconate). Common neonatal patient care activities selected for study were defined according to types of contact22 and included skin contact; respiratory tract care; contact with secretions other than respiratory (ocular, oral, or gastric tubes); change of diapers; manipulation of vascular access devices

(blood sampling or intravenous set connections); and con-tact with equipment related to the neonate (incubator, mon-itor, or ventilator). An observation period started when the observer initiated the structured observation and could include more than one sequence of care. A sequence of care started when the HCW performed hand antisepsis using an alcohol-based handrub and ended when he or she changed activity or reapplied handrub.

Study Procedures

Bacterial contamination of HCWs' hands was assessed as previously described.24 Briefly, two trained external observers conducted structured observation ses-sions during routine neonatal care. During each session, the HCWs activity was interrupted at three points to obtain bacterial samples from the hands: before and after applying handrub and at the end of a sequence of care, but before applying new handrub. When nonsterile dis-posable latex gloves were used during the activity, an imprint of the fingertips was obtained before gloving, after gloving, and at the end of care immediately before and after glove removal. Reliability of data collection has been established in a previous study.24 Collected variables included the day of life of the neonate receiving care; the type and duration of care; and the use of gloves. Observation sessions were randomly distributed accord-ing to the unit workload and covered all shifts. Informed consent was obtained from each HCW before initiation of the observation, and personnel were requested to per-form patient care activities as usual. The study was approved by the institutional review board.

Microbiologic Procedures

Imprints of the five fingertips of the HCWs domi-nant hand were obtained using commercial contact plates

(COUNT-TACT, bioMerieux SA, Marcy l'Etoile, France).

Fingertips were pressed for 5 seconds onto a plate. Plates were transferred to the laboratory, where they were incu-bated at 35° C under aerobic conditions. An initial colony count was performed at 24 hours and a final count at 48 hours of incubation as previously described.24 The maxi-mal colony count was fixed at 300 colony-forming units (CFU); beyond this, growth is confluent and counting is inaccurate. Bacteria were identified by Gram stain, growth on MacConkey agar, API 20 E (bioMerieux SA) profiling, and the slide agglutination test with Pastorex Staph Plus (Bio-Rad, Mannes la Coquette, France) for

Staphylococcus aureus. Statistical Analysis

The main outcome measure was the number of CFU on the ungloved fingertips of the HCWs dominant hand at the end of the sequence of care. Residual bacteria counts after handrub and on gloved fingertips were also assessed as secondary outcomes. A nonparametric regression model (locally weighted regression [LOWESS]) was used to explore the trend in CFU counts according to the dura-tion of each type of care.24 Linear regression was used to model the final bacterial count according to predictors (the type and duration of care and the use of gloves). Explanatory variables with a level of significance of 0.25 or less were entered in a multivariate model. The Wilcoxon signed rank test for paired observation was used for com-parison of bacteria counts before and after applications of handrub. All tests were two-tailed, and the selected thresh-old level for statistical significance was a P value of less than .05. Analyses were conducted using STATA software

(version 7; STATA Corp., College Station, TX). RESULTS

One hundred five structured observation periods, representing a total of 11 hours and 14 minutes, were conducted (median duration, 5.0 minutes; range, 1.5 to 25 minutes) and analyzed during the study. These included 149 sequences of care, 14 with and 135 without the use of gloves (median duration, 3.0 minutes; range, 0.5 to 14 minutes). Observations involved 31% (n = 31) of the HCWs in the neonatal unit. The median age of the neonates being cared for was 13 days (range, 1 to 31 days).

Bacterial Contamination

Of 398 samples from ungloved hands, 360 (90.5%) were culture positive. Skin flora microorganisms (coagu-lase-negative staphylococci, Corynebacterium species, and

Micrococcus species) were isolated in 72.4% of all

positive cultures. Other microorganisms included Enterobacteriaceae (n = 55, 13.8%), S. aureus (n = 10, 2.5%), and filamentous fungi (n = 7, 1.8%). Most Enterobacteriaceae-positive samples (39 of 55) were obtained following the care of neonates older than 14 days. Patient care activities included diaper change (15 of 55), contact with equipment (13 of 55), and respiratory care (11 of 55). Coagulase-negative staphylococci were equally

distrib-194 INFECTION CONTROL AND HOSPITAL EPIDEMIOLOGY March 2004

TABLE 1

BACTERIAL CONTAMINATION OF UNGLOVED HEALTHCARE WORKERS' HANDS DURING 135 SEQUENCES OF CARE AMONG NEONATES NEONATAL U N I T AT THE UNIVERSITY OF GENEVA HOSPITALS, GENEVA, SWITZERLAND, MARCH TO APRIL 2001

Type of Sequence of Care

Median No. (%) Duration (mln) Range of Duration (mln) Increase In Bacterial Count (CFU/mln) C"9. IN THE P Skin contact Diaper change Respiratory tract care

Contact with body secretions other than respiratory

Manipulation of vascular access devices Contact with equipment

Total 27 (20.0) 17 (12.6) 22 (16.3) 23 (17.0) 22 (16.3) 24 (17.8) 135 (100.0) 3.0 4.0 4.0 2.5 5.0 1.5 3.0 1.5 to 11.0 2.0 to 9.5 1.5 to 14.5 1.0 to 10.0 1.5 to 12.5 0.5 to 11.5 0.5 to 14.0 21.2 41.9 37.6 20.1 10.0 9.1 20.4 5.8 to 36.5 28.7 to 55.1 20.4 to 54.82 9.9 to 30.4 2.1 to 18.0 3.1 to 15.2 15.3 to 25.6 .008 <.001 <.001 <.001 .015 <.004 <.001 CFU - colony-forming units; CI95 - 95% confidence interval.

Equipment Vascular Other secretions

3 Li. o 'E 3 e

I

o

Duration of care (min)

FIGURE. Dynamics of bacterial contamination of ungloved healthcare workers' hands in 135 observations according to different patient care activities in

the neonatal unit at the University of Geneva Hospitals, Geneva, Switzerland, from March to April 2001.

uted according to type of contact or neonatal age. All samples from fingertips after glove removal (n = 31) were culture pos-itive with skin flora comprising 84%, Enterobacteriaceae com-prising 12.9%, and S. aureus comcom-prising 3.3%.

Predictors of Bacterial Contamination of HCWs'Hands

On average, a significant increase in bacterial counts (CFU/min) on ungloved HCWs' hands was

observed in all types of care (Table 1). The dynamics of hand contamination showed that after 2 minutes of certain types of contact (skin and diaper change), bacterial counts can be as high as 100 CFU, or even higher during respiratory care (Figure). Neonatal age was not associat-ed with HCW hand contamination (P= .736).

During the 14 sequences with the use of gloves (res-piratory care, n = 6; diaper change, n = 5; and vascular access manipulation, n = 3), a reduced final bacterial count was

TABLE 2

MULTIPLE LINEAR REGRESSION MODEL FOR PREDICTORS OF BACTERIAL CONTAMINATION OF HEALTHCARE WORKERS' HANDS IN 149 OBSERVATIONS IN THE NEONATAL UNIT AT THE UNIVERSITY OF GENEVA HOSPITALS, GENEVA, SWITZERLAND, MARCH TO APRIL

2001

TABLE 3

PREDICTIVE MODEL FOR BACTERIAL CONTAMINATION OF HEALTHCARE WORKERS' HANDS AFTER 3 MINUTES OF PATIENT CARE IN THE NEONATAL UNIT AT THE UNIVERSITY OF GENEVA HOSPITALS, GENEVA, SWITZERLAND, MARCH TO APRIL 2001*

Predictor CFU Count (Cl95) type of Contact Average Increase In CFU Cl„

Contact with equipment Manipulation of vascular

access devices Contact with secretions

other than respiratory Skin contact

Diaper change Respiratory care Use of gloves Duration of care, min

CFU = colonyforming units; CL,5

-3.6 (-28.0 to 35.2) -2.9 (-43.7 to 37.9) 32.7 (-8.3 to 73.6) 58.8 (18.6 to 98.9) 81.8 (39.6 to 124.0) 98.9 (57.7 to 140.1) -64.5 (-107.0 to -22.1) 15.3 (10.9 to 19.7) 95% confidence interval. .820 .890 .120 .004 <.001 <.001 .003 <.001

Contact with equipment Manipulation of vascular

access devices With gloves Without gloves Contact with secretions

other than respiratory Skin contact Diaper change With gloves Without gloves Respiratory care With gloves Without gloves 49.54 -17.87 46.67 82.22 108.31 66.83 131.36 83.89 148.43 18.65 to 80.43 -64.50 to 28.74 19.40 to 73.94 54.42 to 110.02 81.50 to 135.12 23.25 to 110.41 72.48 to 190.25 40.96 to 126.82 120.26 to 176.57

observed on the ungloved fingertips as compared with sequences involving the same types of contact during which gloves were not used. HCWs who did not wear gloves acquired, on average, 24.5 CFU/min (95% confidence inter-val [ C I J , 16.2 to 32.8 CFU/min; P < .001) as compared with -1.9 CFU/min (CI^, -11.5 to 7.7 CFU/min; P = .690) among those who did. However, glove contamination was clearly demonstrated during respiratory care (16.7 CFU/min; CIg5,

0.6 to 32.8 CFU/min; P = .043) and diaper change (78.3 CFU/min; CI<,5, 47.5 to 109.1 CFU/min; P< .001).

Multivariate Model

The type and duration of care and the use of gloves significantly predicted bacterial hand contamination (Table 2). Whereas the use of gloves protected the hands of HCWs from bacterial contamination, skin contact, diaper change, and respiratory care were associated with a significant increase in bacterial contamination. In a predictive model using the median duration of the sequence of care (3 min-utes) , all types of contact were associated with a significant increase in bacterial counts, with the exception of the manip-ulation of vascular access devices with the use of gloves (Table 3). Although the average bacterial counts were lower when gloves were used, a significant increase in CFU counts was still observed on hands following glove removal during diaper change and respiratory care.

Effect of Handrub

We measured bacterial counts on fingertips before and after the application of handrub in 93 episodes of hand antisepsis. Bacterial contamination was significantly reduced following handrub; median CFU counts before and after hand antisepsis were 61 (range, 0 to 300; interquartile range, 10 and 281) and 4 (range, 0 to 209; interquartile range, 1 and 14; P < .001), respectively. This

CFU = colony-forming units; CL,5 = 95% confidence interval.

*Multiple linear regression.

reduction was independent of the type of bacterial conta-mination: skin flora microorganisms (P = .003); Enterobacteriaceae (P= .004); and S. aureus (P= .030).

D I S C U S S I O N

Our study showed that all types of care that did not include the use of gloves were associated with a signifi-cant increase in the bacterial contamination of HCWs' hands. Therefore, it seems that the term "clean" care, as it has been proposed,2122 may no longer be appropriate. To our knowledge, this is the first study to evaluate the degree of hand contamination of HCWs during routine neonatal care. The presented data show a clear grading of the relative potential for bacterial hand contamination among different types of patient and environmental con-tacts in the neonatal setting, thus identifying key opportu-nities for hand hygiene. This information may also prove to be useful for future neonatal care planning.

Many guidelines,20 including a newly developed set,18 recommend hand hygiene between different care activities for the same patient, but few studies have evalu-ated this grading in terms of bacterial burden. In a previ-ous study performed in all wards in our institution, the patient care activities that were independently associated with higher contamination levels of HCWs' hands were respiratory care, direct patient contact, and handling of body fluid secretions.24 In the current study, we selected activities from the daily neonatal scenario and individual-ized them in sequences of care. This approach enabled the evaluation of the dynamics of hand contamination dur-ing routine neonatal care. Although diaper change,

respi-196 INFECTION CONTROL AND HOSPITAL EPIDEMIOLOGY March 2004

ratory care, and handling of secretions (other than respi-ratory) all refer to contact with body fluid secretions, these activities are closely linked to the routine care of neonates. Most neonatal care activities are highly inte-grated and involve skin contact; however, our aim was to evaluate to what extent other activities differed from pure skin contact in terms of potential for bacterial hand conta-mination. Despite the brief nature of neonatal care, we found that defined acts such as diaper change and respi-ratory care were associated with a rapid increase in bac-terial counts, strongly suggesting that hand hygiene should be performed before moving to another body site for care of the same patient.

The previously reported protective effect of gloves against bacterial contamination24"26 was confirmed in the current study in the multiple regression model. Glove use protected hands better during the manipulation of vascular access devices than during diaper change or res-piratory care. This could have been due to a smaller bac-terial load on gloved hands with less hand contamination during glove removal.27,28 Importantly, our study showed that both commensal and pathogenic bacteria accumulate on gloves during the process of care. Possible lack of glove removal during patient care has been associated with outbreak situations.29 Although gloves protect their hands from bacterial contamination, HCWs must be aware that contaminated gloves may facilitate cross-transmission when not appropriately removed, particu-larly following activities associated with high bacterial load. Our findings strengthen the recent suggestions to promote hand hygiene action immediately after glove removal and to change gloves between care at different body sites for the same patient.18

Although the level of bacterial contamination on hands after contact with the close environment was lower than that after most direct patient contact, it was nonethe-less significant. It has already been reported that HCWs' hands may become contaminated after contact with inani-mate surfaces,30"32 and the environment has been sug-gested as a possible reservoir for nosocomial pathogens in the hospital setting.32 None of these studies, including the current one, were designed to evaluate whether such contamination could result in pathogen transmission to susceptible patients. However, contact with a contaminat-ed environment may play a role in high-risk newborn nurseries or neonatal intensive care units, particularly regarding bacteria that can survive for prolonged periods in inanimate environments.33

This study has several limitations. First, there is a lack of causal association between the dynamics of hand contamination and the risk of healthcare-associated infec-tion among neonates. Further studies are needed to eval-uate this link. Second, the method has limitations in that the number of bacteria expressed does not reflect total contamination, as part of the contaminating bacteria stays adhered to the skin. This has been shown under laborato-ry conditions by repetitive sampling of finger imprints. However, this method has been shown to be a reliable

indicator of transient contamination. The alternative glove-juice method as described in the American Society for Testing and Materials Standard E1174-00 could not be adapted to our study because the study design required interruptions in the sequence that made its application unfeasible.34

We have shown that hands become rapidly contam-inated with commensal flora and, at times, with potential pathogens during routine neonatal care, reinforcing the need for hand antisepsis during the sequence of patient care or before starting a different task. The current study has also shown that bacteria accumulate on and beneath gloves during patient care and that gloving does not fully prevent hand contamination, thus emphasizing the need for hand antisepsis after glove removal. Neonates repre-sent a particularly vulnerable population for infection, and there is a need to identify key care activities and actions for which hand hygiene is essential to prevent pathogen transmission. An awareness of this grading may help HCWs achieve compliance in a realistic manner.

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